Prevalence of Gastrointestinal Parasites and Efficacy of Anthelmintics Against Nematodes in Camels in Yabello District, Southern Ethiopia

Acta Parasitologica Globalis 5 (3): 223-231, 2014 ISSN 2079-2018 IDOSI Publications, 2014 DOI: 10.5829/idosi.apg.2014.5.3.85129 Prevalence of Gastrointestinal Parasites and Efficacy of Anthelmintics Against Nematodes in Camels in Yabello District, Southern Ethiopia Kasahun Demelash, Fikadu Alemu, Ayalew Niguse and Teka Feyera Jigjiga University College of Veterinary Medicine, Ethiopia Abstract: A study, that comprised of cross sectional study and controlled field trial, was conducted from December 2013 to April 2014 with the objective of estimating the prevalence of gastrointestinal parasites in randomly selected 384 camels (Camelus dromedaries) and testing the efficacy of three anthelmintics, namely ivermectin, albendazole and levamizole against nematodes in camels in Yabello district, Southern Ethiopia. For the prevalence study, fresh faecal sample obtained from each animal was screened for the presence of gastrointestinal (GI) parasites egg using faecal floatation and sedimentation, whereas infestation burden was determined by McMaster egg counting technique. Camels which had moderate to heavy egg counts (EPG of more than 400) were selected and used for the anthelmintics efficacy study. This included three treatment and one negative control groups. Out of the 384 camels examined, 310 (80.73%) were found to harbor different GI parasites. The result showed that 79.67% of eggs identified were those of Trichostrongylus followed by Strongyl species (59.67%).There was a statistically significant difference in the prevalence of GI parasites between age groups and origin of animals (p<0.05) but not between the different body condition and sex groups. On the other hand, the degree of GI parasitic infestation between sex and age groups differed statistically (p<0.05) but no significant difference between the body condition groups. The efficacy study, as measured by feacal egg count reduction percentage (FECR %), also evidenced that of the three drugs studied, ivermectin at a dose of 0.2 mg/kg and albendazole at a dose of 10 mg/kg substantially reduced nematode egg counts post-treatment. Although slightly lower, levamizole (at a dose of 10 mg/kg) also considerably reduced the parasite burden. Taken as a whole, the present study established that camels in Yabello district harbor different GI parasites which could hamper health and production status of this subject. Ivermectin and albendazole showed a promising efficacy against nematodes and can still be considered as appropriate chemotherapeutic options for control of GI parasitosis in Camel. Key words: Anthelmintic Camel Efficacy Faecal Egg Count Reduction Nematode Prevalence INTRODUCTION pastoral community is highly considerable and so many families depend on this species for their daily needs. The camel (Camelus dromedaries) is an important However, camel production is practiced by pastoral livestock species uniquely adapted to hot arid communities under diverse constraints in dry and environments. World camel population is estimated to be marginal areas. Infectious and parasitic diseases appear around 25.89 million across 47 countries. About 85% of to be the major constraints that are hampering the the camel population inhabits mainly eastern and northern potential performances of the animals. In Ethiopia, Africa and the rest in Indian subcontinent and Middle gastrointestinal parasites are one of the major obstacles East countries [1]. In Ethiopia, camels represent a subset in the growth and development of animal health. of major livestock resources with a population estimated Factors like constant exposure to parasitic infestation at >2.4 million [2]. include variable geo-climatic condition, shortage of The major ethnic groups owning camels in Ethiopia food and lack of knowledge of farmers in treating GI are the Beja, Rashaida, Afar, Somali and Borena [3]. parasites play an important role in proliferation of the The role of camels towards milk and meat production at parasites and their diseases [4]. Corresponding Author: Teka Feyera, Jigjiga University College of Veterinary Medicine, Ethiopia, P.O. Box: 1020. 223

The demands of maximizing production have led Each group was then randomly allocated into one of the today s beef and dairy producers to adopt preventive three (Table 1) anthelmintics groups and one untreated control measures that include regular treatment of their control group. livestock with anthelmintics during the grazing season. All the evaluated anthelmintics were imported into The management approach combined with environmental the country by registered companies that are licensed to factors, the use of more efficacious anthelmintics and their distribute veterinary drugs. All the drugs were used dosing practices are believed to reduce parasitic within their expiry date and stored as per instructions of resistance against anthelmintics. Anthelmintic resistance the manufacturers. The details of anthelmintics used for in camel is becoming a problem as of other livestock [5]. the efficacy study are given in Table 1. But, until recently, there was little or no documented The animals were treated with the respective research on parasite resistance and comparative efficacy anthelmintics dosage as per the recommendations of the to commonly used anthelmintics in Ethiopia in general and manufacturers according to the weight of individual in the current study area in particular. This work, animal. Then the efficacy of this three selected drugs therefore, aimed at estimating the prevalence of against nematode parasites of camel in each group was gastrointestinal parasites in live camels of Yabello woreda evaluated and interpreted in accordance with the and evaluating the efficacy of commonly used guidelines provided by World Association for the anthelmintic drugs against nematode parasites in camels. Advancement of Veterinary Parasitology (WAAVP) recommendation for efficacy evaluations of anthelmintics MATERIALS AND METHODS [7]. On the basis of these guidelines, efficacy of anthelmintics against nematodes was evaluated based Description of the Study Area: The study was conducted on FECR percentage which was calculated as: from December 2013 to April 2014 in Yabello woreda, FECR%=100(1-T2/T1*C1/C2), Where T and C represent Southern Ethiopia. Yabello town is geographically located treated and control groups respectively, while the at an altitude of 1000-1500m above sea level at a distance subscripts 1and 2 represent pre- and post-treatment of 565km from Addis Ababa. The mean annual minimum respectively. Here resistance is considered to be present and maximum temperatures are 24 c and 29 C respectively. if the FECR% is less than 90% [7]. The climate is generally semi-arid with annual average rainfalls ranging from 300 mm in the South to >700 mm in Sample Size Determination: The number of animals to be the North [6]. sampled for the epidemiological study was estimated by the formula described by Thrusfield [8]. Study Population and Sampling Methods: The study 2 populations were camel herds from four randomly selected 1.96 (Pexp (1- Pexp)) N= 2 kebeles/peasant associations (PAs), of Yabello woreda. d Villages in each kebele were selected as sampling unit and where N is number of animals to be sampled, P is the villages herds were selected and investigated. For the expected prevalence of the disease and d is precision level prevalence study, a total of 384 animals, of all age groups (0.05). Since there was no any previous study on and both sex (91 from Dida Hara, 106 from Derito, 75 from gastrointestinal parasites prevalence in the study area, DidaYabello and 112 from Chorkasa) were randomly 50% was used as expected prevalence of the disease. selected from different herds. The criteria for inclusion in Accordingly, the estimated sample size was 384. the controlled field trial were history of anthelmintics usage, owners willingness and parasite burden (EPG) of Sample Collection and Examination: Fecal samples were greater than or equal to 400 in prevalence study. collected directly from the rectum of all camels in separate polyethylene bags and examined for the presence of ova Study Design: The study employed a cross-sectional by using a simple test tube flotation and sedimentation study design for estimation of prevalence and a controlled techniques described by Hansen and Perry [9]. field trial for anthelmenthics efficacy test. All animals Identification of eggs of each species of camel parasites selected for anthelmintics efficacy trial from the four PAs was done according to the procedure described by were allocated into 4 groups of 8 animals each by blocking Soulsby [10]. For the efficacy study, nematode ova using feacal egg count (FEC) conducted before treatment positive camels were divided into four groups consisting so that the mean FEC per each group was fairly uniform. of three treatment and one control groups. Examination of 224

Table 1: Details of anthelmintic drugs used for the efficacy evaluation Trade name Generic name Manufacturer Dosage Route Expitol Albendazole ERFAR 7.5mg/kg Oral Noromectin Ivermectine Nor brook laboratories 0.2mg/kg SC Terazole Y Levamizole Ashish life science 7.5mg/kg Oral SC= sub-cutaneous fecal samples was done during pre-medication (Day 0) The likelihood that camel was positive for GIT and approximately on day 14 post-medication for all parasite eggs varied significantly with administrative groups of ova positive camels. The treatment groups location. Camels located in DidaYabello and Derito PAs received antihelminthic drugs, whereas the negative had significantly higher prevalence of helminth eggs than control remained untreated. animals located in Dida Hara and Chorkasa (p<0.05) (Table 6). Body condition score was not significantly Data Analysis: Data analysis was done using SPSS associated with prevalence of parasite infestation version 16 software program. Associations between (p>0.05). parasitism and categorical (Age groups, sex, body condition score (BCS) and area of origin) factors were Efficacy Study Results: The results of the mean FEC for compared using chi-square tests for independence. the treated and control groups and the percentage feacal The level of significance was set at p<0.05. For the egg count reduction (FECR) in the treated groups for each experimental study, efficacy of anthelmintics used was anthelmintic drug tested are shown in Table 7. No or evaluated by calculating FECR % using the formula, considerably few parasite eggs were recorded FECR %=100 (1-T2/T1*C1/C2) and resistance against the th approximately on the 14 day post-treatment in the drugs was set at FECR value of <90% [7]. treatment groups, except in camels treated with levamizole. There was a substantial reduction in the FEC with all the RESULTS anthelmintics tested against nematodes. The feacal th examination on the 14 day post-treatment revealed a very Prevalence of Gastrointestinal Parasites: A total of 384 high efficacy (93 to 100% FECR) particularly in ivermectin camels were examined, of which 310 (80.73%) were and albendazole treated groups. diagnosed as harboring Nematode, Trematode, Ceastode and Protozoan eggs at varying levels. The proportion of DISCUSSION camels harboring nematode eggs was considerably high in which Trichostrongylus is the most prevalent (79.67%), Prevalence Study Output: The present work revealed followed by strongly spp. (59.67%), Nematodirus an overall GI parasites prevalence of 80.73% in camels. (56.77%), Strongyloides (26.56%) and Trichuris (0.64%). Eight different species of gastrointestinal tract worms Other gastro-intestinal parasite eggs encountered include; and protozoa were identified in camels. They were Trematodes (Paraphistomum, 21.61%), Ceastodes broadly classified as Nematodes (6 species), Trematodes (Monesia, 10.64) and Protozoan Oocysts (Eimeriaspp, (1 species) and protozoan (1 species) and Ceastode 51.4%). Regarding type of infestation, single parasite (1 species) according to the egg morphology [11]. infestation (n=30; 7.8%) was lower than mixed infestation The relatively high level of endoparasitosis recorded (Two (74; 19.3%) or three (115; 29.9%) or four (64; 16.7%) in this study is probably related to the number of adult and five (27, 7%)) parasite infestation (Tables 2 and 3). parasites established in the GIT, level of host immunity, There was no significant difference (p>0.05) in stage of parasite infection and lack of improvement in probability of being infected by helminthes between male animal health management programs or non-adoption of and female camels (Table 4). But there was significant the modern animal health care programs by camel owners. difference (p<0.05) between infected male and female This finding is in agreement with the 81.31% report camels in severity of infection (EPG), females being by Anvari-Tafti et al. [12], 75.1% by Borji et al. [13] severely infected than males (Table 5). Host age was (In Iranian camels and75% by Bekele [14] (In Eastern found to be a significant factor for the prevalence of Ethiopia) and 78.0% by Mahmud et al. [15] in Sokoto GI parasites (p<0.05), with eggs/oocysts being detected metropolis. However, it was relatively lower than the more frequently in age categories >6 years than <3 years prevalence rates in Jordan (98%) by Sharrif et al. [16], and 3-6 years (Table 6). Eestern Ethiopia (96.92%) [17] and Nigeria (92.4%) [18]. 225

Table 2: Prevalence of individual GI parasites in both single and mixed infestation Parasite class Parasite spps Number positive Prevalence (%) Nematodes Trichostrongylus 247 79.67 Strongly Spps. 185 59.67 Nematodirus 176 56.77 Strongyloides 102 32.9 Trichuris 2 0.64 Ceastode Monesia 33 10.64 Trematodes Paraphystomum 67 21.61 Protozoan Coccidia 159 51.29 Table 3: Prevalence of GI parasites observed in mixed and single infestation Parasite Sex Mixed infestation Male Female Total (prevalence) Two parasite 23(19.49%) 51(19.17%) 74(19.27%) Three parasite 32(27012%) 83(31.20%) 115(29.95%) Four parasite 15(12.71%) 49(18.42%) 64(16.67%) Five parasite 7(5.93%) 20(7.52%) 27(7.03%) No parasite 29(24.58%) 45(16.92%) 74(19.27%) Single infestation Coccidia 3(2.54%) 4(1.5%) 7(1.82%) Nematodirus 0(0.00%) 1(0.38%) 1(0.26%) Strongly spps 1(0.85%) 0(0.00%) 1(0.26%) Strongyloides 1(0.85%) 1(0.38%) 2(0.52%) Trichostrongylus 7(5.93%) 12(4.51%) 19(4.95%) Total 118(100%) 226 (100%) 384(100%) Table 4: Prevalence of GI parasites in relation to age, sex and body condition score as risk factors Risk factor Total animals examined No. of positive (prevalence) 2 P-value Sex Male 118 89(75.42) 3.0821 0.079 Female 266 221(83.08) Total 384 310(80.73) Age <3yrs (young) 89 64(71.91) 7.33 0.026* 3-6 yrs. (adult) 91 72(79.12) >6yrs (old) 204 174(85.29) Total 384 310(80.73) BCS Good 226 211(79.32) 1.3895 0.499 Medium 104 88(84.62) Poor 14 11(78.57) Total 384 310(80.73) *= p<0.05 In contrast, it was greater than the prevalence rate of the most incriminated helminths in camels [24]. In the 68.9% reported in Nigeria [19].The country to-country present study, out of the 384 dromedaries examined, variation can be adequately attributed to variation 70.29% were found infested with nematodes. This is in between agro-climatic conditions, levels of hygiene and agreement with the report of Mohamed et al. [21] (69%) husbandry practices. The same reason was suggested by in Egypt. In Eastern Ethiopia, Bekele [14] and Abebe [25] Allport et al. [20] and Mohamed et al. [21]. has reported prevalence rates of 91.5% and 87%, Mixed parasitism (90.3%) involving two or more respectively, which were higher than the present finding. helminth genera were common in the present study This may be attributed to the difference in sampling and was greater than the results of other researchers period of the year and duration of the study; the same [14, 22, 23]. Trichostrongylus species and Strongylus were reason was given by Mohamed et al. [21]. 226

Table 5: Degree of GI parasitic infestation in relation to different risk factors Variables Degree of infestation Sex Light Moderate Heavy 2 P value Male 29(24.58) 37(31.36) 23(19.49) Female 47(17.67) 88(32.08) 86(32.33) 9.28 0.026* Total 76 125 109 Age <3yrs (young) 14(15.73) 22(24.72) 28(31.46) 3-6yrs(adult) 20(21.98) 39(42.86) 13(14.29) 20.1097 0.003* >6yrs(old) 42(20.59) 64(31.37) 68(33.33) Total 76 125 109 BCS Good 53(19.92) 90(33.83) 68(25.56) Medium 21(20.19) 29(27.88) 38(36.54) 6.0543 0.417 Poor 2(14.29) 6(42.86) 3(21.43) Total 76 125 109 *= p<0.05; BCS= body condition score Table 6. Prevalence of GIT parasites in association with origin of camels as risk factor Pas Total animal examined No. of positive (prevalence) 2 P-value D/hara 91 69(75.82%) Derito 106 98(92.45%) 16.0423 0.001* D/Yabello 75 62(82.67%) Chorkasa 112 81(72.32%) Total 384 310(80.73%) *= p<0.05, PA= peasant association Table 7: Comparative Fecal Egg Count Reduction (FECR) test using arithmetic means 7a. Ivermectin Group Parasite Number affected EPG at day 0 EPG at day 14 (% reduction) Trichostrongylus 1 700 0.00 (100%) Trichostrongylus + Nematodirus 2 1400 0.00 (100%) Trichostrongylus+Stronglyspps. 2 28000 350 (93.42%) Trichostrongylus + Strongyloides 1 1800 200 (96.29%) Trichostrongylus +Nematodirus +Strongyl spp. 1 700 0.00 (100%) Trichostrongylus + Nematodirus+ Strongyloides 1 700 0.00 (100%) Mean 1012.5 68.75 (94.02%) EPG= Egg per gram 7b: Albendazole Group Parasite Number affected EPG at day 0 EPG at day 14 (% reduction) Trichostrongylus 2 2300 200 (94.46%) Trichostrongylus+ Nematodirus 2 2600 100 (96.48%) Trichostrongylus + Strongyloides 1 2000 100 (97.36%) Trichostrongylus+Nematodirus +Strongyloides 1 2400 100 (98.6%) Strongly Spps 1 400 0.00 (100%) Trichostrongylus + Nematodirus +Strongly spps. 1 1800 100 (96.22%) Mean 1437.5 75 (93.4 EPG= Egg per gram 227

7C: Levamizole Group Parasite Number affected EPG at day 0 EPG at day 14 (% reduction) Trichostrongylus 3 2800 500 (88.63%) Trichostrongylus + Nematodirus 1 500 0.00 (100%) Trichostrongylus + Strongyloides 1 800 100 (93.42%) Nematodirus + Strongly spps. 1 700 100 (95.23%) Trichostrongylus + Nematodirus + Strongyloides 1 1400 400 (87.3%) Trichostrongylus + Nematodirus + Strongylspps. 1 3700 800 (85.58%) Mean 1237.5 237.5 (79.34%) EPG= Egg per gram 7d: Untreated Control Parasite Number affected EPG at day 0 EPG at day 14 (% reduction) Trichostrongylus + Nematodirus + Strongylspps. 1 700 1100 Trichostrongylus + Nematodirus 3 2100 3200 Trichostrongylus + Nematodirus + Strongyloides 1 1000 1900 Trichostrongylus 1 300 900 Strongyloides 1 400 900 Strongylspps. + Strongyloides + Nematodirus 1 800 1200 Mean 662.5 1150 EPG= Egg per gram Most of the researchers have observed higher rates The most probable reason for this could be the difference of parasite infestation/worm burden in female hosts in microclimates of the localities. compared with the males [26-28]. However, Gulland and The study further revealed that body conditions of Fox [29] reported that prevalence and intensity of the animal did not show significant association with the infection (feacal egg counts) were higher in males than prevalence of the parasites. The absence of association females, except during the lambing periods. But the between body condition and prevalence disagrees with present study revealed that there was no significant previous reports in other livestock species [31]. This difference (p>0.05) in prevalence of parasite between male could be explained by the fact that loss of body condition and female, however intensity of infections showed in the study animals could be due to other factors such as significant association with sex showing high feacal egg seasonal change of forgeable feedstaff and the presence count in female than in male (p<0.05). This could be of other concurrent disease conditions, mainly high attributed to the fact that female animals are highly prevalence of trypanosomiasis, as the study was suffered by stresses that may lower their immunity than conducted in some of the lowland areas [22]. males even if they have equal option of exposure to parasite infection with male. Efficacy of Anthelmintics: The result of FECR test The analysis result also revealed that the average age showed that there were marked decreases in EPG due to of the infected camels was significantly higher than treatment in all of the three anthelmintics used in this trial. non-infected camels and there was a significant However, the degree of EPG decrement in each association (p<0.05) between the age and the severity of anthelmintic was different. The mean EPG of feaces which infection. An age dependent acquiring resistance to was 1012.5, 1437.5 and 1237.5 in ivermectin, albendazole gastrointestinal parasites has been proven in some and levamizole treated group respectively before species [30]. The present result did not show a similar age treatment were decreased to 68.75, 87.5 and 237.5 in dependent resistance in camels in the study area. It seems ivermectin, albendazole and levamizole treated group post that the increase in age of the camels is associated with treatment (As indicated in Table 6, 7 and 8). The study the increase in the chance of parasitic encounter along revealed a relatively higher EPG reduction in ivermectin with the decrease in body immunity against infestation. and albendazole treated groups. Those treated with There is a significant difference in the prevalence of levamizole also showed considerable reduction in EPG most of the helminths among the four PAs. Camels values although slightly lower than the observation in the located in DidaYabello and Derito kebeles had former two drugs. This may be due to the slow and significantly higher prevalence of helminth eggs infection inconsistent action of the drug. The same reason was than animals located in Dida Hara and Chorkasa (p<0.05). suggested by Mukhwana and Mitema [32]. 228

The fecal egg count reduction percentage of all that ivermectin and albendazole showed a relatively anthelmintics in the present study were ranging from higher efficacy, as measured by FECR%, in controlling 93-100,with the mean being 94%, 94-100 with the mean camel nematodes than levamisole. Thus, Strategic being 93.478% and 85-100 mean remain 79.5% in deworming of camels using broad-spectrum anthelmintics ivermectin, albendazole and levamizole respectively. (Such as ivermectin and albendazole) could be This result is relatively in line with the report of implemented to increase the productivity of camels. Mahfooz et al. [33] who reported a FECR% ranging from 95.76 to 99.38 in ivermectin therapy with the mean REFERENCES reduction percentage being 97.31%. The observation in the current study would seem to suggest that ivermectin 1. FAO (Food and Agriculture Organization of the and albendazole are relatively more efficacious in United Nations), 2008. Production Yearbook, Volume controlling camel GI nematodes than levamizole as 56. Rome, Italy. revealed by FECRT. A similar observation was made by 2. Central Statistical Authority, 2009. Agricultural Brander et al. [34]. sample survey (2008/2009). Statistical bulletin 302, Despite this effectiveness, some parasites survived Addis Ababa, Ethiopia. the treatment even if their egg count were reduced to the 3. Workneh, N., 2002. Socio-economic importance of level of few EPG count. The two nematode parasite camel in Ethiopia: An overview. A paper presented species recovered from all experimental animals were on the international workshop on Camel Research Trichostrongylus and Strongyl spps. This could be and Development: Formulating a Research ascribed to the fact that these parasites are the first and Agenda for the Next Decade, Wad Medani, Sudan, the second most prevalent nematodes in the study area pp: 9-12. which might have led them to adapt the frequently used 4. Durrani, A.Z., 1991. Faecal culture technique, MSc anthelmintics resulting in development of resistance. (Hons) Thesis, University of Agriculture, Faisalabad, Achenef et al. [35] made a similar observation and Pakistan. deduced the possibility of anthelmintics adaptation and, 5. Ballweber, L.R., 2009. Ecto- and Endoparasites of thus, resistance. camelids. Veterinary Clinics of North America Food CONCLUSION 6. Animal Practice, 25: 295-310. Borana Zone Department of Planning and Economic Development, 1998. The present study conducted in Yabello woreda 7. Coles, G.C., C. Bauer, F.H.M. Borgsteede, S. Geerts, showed that camels of the area harbor different T.R. Klei, M.A. Taylor and P.J. Waller, 1992. World gastrointestinal parasites that could have enough Association for the Advancement of Veterinary implication on the health and production status of the Parasitology (WAAMVP). Methods for the detection animals. In the current study the prevalence of GI of anthelmintic resistance in nematodes of veterinary parasitosis was 80.73% from which nematodes accounted importance. Veterinary Parasitology, 44: 35-44. the highest number. The study also revealed that mixed 8. Thrusfield, M.V., 2005. Veterinary Epidemiology, infestation was more common in the area covering 90.3% rd 3 ed., Blackwell Science, Oxford, London, UK, of the total prevalence than single infestation which was pp: 234-238. only 9.67%. It was also evidenced that body condition 9. Hansen, J. and B. Perry, 1994. The epidemiology, score and sex as risk factors did not have significant diagnosis and control of helminth parasite of association with the prevalence, while age and area of nd ruminants 2 ed. Nairobi, Kenya. origin were significantly associated with the GI 10. Soulsby, E.J.L., 1982. Helminths arthropods and parasitosis. But the study showed that severity of the th protozoa of domesticated animals.7 ed. London. infestation was significantly different among age, sex and BailliereTindall, pp: 231-250. areas of origin. The controlled field trial in the study 11. Max, R.A., A.F. Vatta, M.L. Jayaswal, A.E. Kimambo, indicated that there was marked decrease in EPG count in A.A. Kassuku and L.A. Mtenga, 2006. Technical treated camels after about 14 days of treatment as manual for worm management in small ruminants, compared with untreated group. The study also revealed Sokoine University of Agriculture Tanzania, pp: 2-4. 229

12. Anvari-Tafti, M., A. Sazmand, S. Hekmatimoghaddam 22. Swai, S., W. Moshy, D. Mshanga, J. Lutatina and I. Moobedi, 2012. Department of Pathobiology, and S. Bwanga, 2011. Intestinal parasitic School of Medicine, ShahidSadoughi University of infections of camels in the agro and pastoral Medical Sciences, Yazd, Iran. areas of northern Tanzania Veterinary Investigation 13. Borji, H., G.R. Razmi, A.R. Movassaghi, A. Naghibi Centre. and M. Maleki, 2010. A study on 23. Tembely, S., P.A. Diarra and Y. Waigalo, 1992. gastrointestinal helminths of camels in Mashhad Preliminary observations on helminth parasite Abattoir, Iran. Iranian Journal of Veterinary Research, populations of the dromedary in northern Mali. 11: 174-179. Veterinary Parasitology, 44(3-4): 339-342. 14. Bekele, T., 2002. Epidemiological studies on 24. Rewatkar, S.G., S.S. Deshmukh, S.K. Deshkar, gastrointestinal helminths of dromedary in semi-arid D.K. Maske, P.D. Jurnde and G.N. Bhangale, 2009. lands of eastern Ethiopia. Veterinary Parasitology, Gastrointestinal helminthes in migratory camel, 105: 139-152. Veterinary World Journal, 2(7): 258. 15. Mahmud, A., A.A. Mohammed, M.O. Alayande, 25. Abebe, W., 1991. Traditional husbandry practices Y.I. Habila, M.D. Lawal, M. Usman, A.A. Raji, and major health problems of camel in the Ogaden. B. Saidu, M.S. Yahaya and N. Suleiman, 2014. Nomadic Peoples, 29: 21-30. Prevalence and distribution of gastrointestinal 26. Maqsood, M., Z. Iqbal and A.H. Chaudhry, 1996. parasites of working camels in Sokoto metropolis. Prevalence and intensity of Haemonchosis with Veterinary World, 7(3): 108-112. reference to breed, sex and age. PakistanVetetrinary 16. Sharrif, L., K.M. Al-qudah and F.K. Al-Ani, 1997. Journal, 124: 177-195. Prevalence of gastrointestinal helminthes in 27. Komoin, O.C., J. Zinsstag, V.S. Pandey, F. Fofana and one-humped camel in Jordan. Journal of Camel A.N. Depo, 1999. Epidemiology of parasites in Practices and Research, 41: 67-69. southern forest zone of Coted Ivoire. Revue- 17. Tekle, T. and G. Abede, 2001. Trypanosomosis and d Elevage-etde-MedecineVeterinaire-des-Payshelminthoses: major health problems of camels Tropicaux, 52(1): 39-46. (Camelusdromedarius) in the Southern Rangelands of 28. Valcarcel, F. and C.G. Romero, 1999. Prevalence and Borena, Ethiopia. Journal of Camel Practice and seasonal pattern of Trichostrongylus in a dry area of Research, 8(1): 39-42. central Spain. Journal of Veterinary Medicine Series, 18. Bamaiyi, P.H. and A.U. Kalu, 2011. Gastrointestinal 46(10): 673-681. parasites infection in one humped camels of Nigeria. 29. Gulland, F.M.D. and M. Fox, 1992. Epidemiology of Veterinary Research Forum, 2(4): 278-281. nematode infections of Soay on St. Kilda. 19. Kamani, J., A.U. Turaki, G.O. Egwu, A.U. Mani, Parasitology, 105(3): 481-492. S.M. Kida, J.G. Abdullahi, M.S. Damina, 30. Silva, W.W., C.M.L. Bevilaqua and A.L. Costa, 1998. H.A. Kumshe and G.I. Dogo, 2008. Prevalence of Natural evolution of gastrointestinal nematodes in gastrointestinal parasites in camels (Camelus goats in the semi-arid ecosystem of the Paraiba dromedaries) slaughtered in Maiduguri, Nigeria. backwoods, northeastern Brazil. Veterinary Journal of Camel Practices and Res., 15(2): 181-182. Parasitology, 80: 47-52. 20. Allport, R., R. Mosha, M. Bahari, E.S. Swai and 31. Keyyu, J.D., A.A. Kassuku, N.C. Kyvsgaard and A. Catley, 2005. The use of community-based A.L. Willingham, 2003. Gastrointestinal nematodes in animal health workers to strengthen disease indigenous zebu cattle under pastoral and nomadic surveillance system in Tanzania. Revue scientifiqueet management systems in the lower plain of Southern technique International Office of Epizootics, highlands of Tanzania, Veterinary Research 24(3): 921-932. Communication, 27(5): 371-380. 21. Mohamed, A.M., R. Mahmoud, G.A. Abdella and 32. Mukhwana, E.J. and E.S. Mitema, 1997. Comparative Abou, El-Ella, 2008. The influence of Some Nematode efficacy of three anthelmintics against mixed GIT Parasitism on Lipid Metabolism and Lipoprotein nematode infection in camels. Univ. of Nairobi, Profile in Dromedary Camel. Journal of Camel Science, Kenya. Tropical Animal Healthand Production pp: 63-67. Journal, 29: 99-101. 230

33. Mahfooz, A., M. Abubakar, Q. Bilal and T. Ahmad, 35. Achenef, M., B. Basaznew, C. Mersha, F. Tewodros 2006. Prevalence and chemotherapy of GIT parasites and B. Ayalew, 2013. Study on utilization and in camels in and around Faisalabad, Pakistan. efficacy of commonly used anthelmintics against Department of clinical medicine and surgery, Pakistan gastrointestinal nematodes in naturally infected Veterinary Journal, 26(4): 209-210. sheep in North Gondar, African Journal of 34. Brander, G.C., D.M. Puch, R.J. Bywater and Pharmacology, 7(12): 679-684. W.L. Jenkins, 1991.Anthelmintics, in veterinary th applied pharmacology and therapeutics, 5 ed. pp: 470-502. 231